J Appl Physiol 98: 2101–2107, 2005.
First published January 27, 2005; doi:10.1152/japplphysiol.00784.2004.
Effects of two cooling strategies on thermoregulatory responses of tetraplegic
athletes during repeated intermittent exercise in the heat
N. Webborn,1,2 M. J. Price,3 P. C. Castle,1 and V. L. Goosey-Tolfrey2,4
1
Department of Sport and Exercise Science, University of Brighton, Eastbourne; 2British Paralympic
Association, Croydon, Surrey; 3School of Science and the Environment, Coventry University,
Coventry; and 4Centre for Biophysical and Clinical Research into Human Movement, Department
of Exercise and Sport Science, The Manchester Metropolitan University, Alsager, United Kingdom
Submitted 26 July 2004; accepted in final form 21 January 2005
SPINAL CORD INJURY RESULTS in reduced vasomotor and sweating
responses below the level of lesion with subsequent thermoregulatory dysfunction (12). Studies of paraplegic individuals
at rest and during exercise have shown that thermoregulatory
responses are proportional to the level of lesion, reflecting the
amount of sympathetic nervous system available for sweating
and blood redistribution (12, 22, 26). However, when the level
of spinal cord lesion is in the cervical region resulting in
tetraplegia (also known as quadriplegia), much greater thermal
strain is observed during both resting and exercise heat exposure (12, 26). For example, during resting heat exposure,
tetraplegic individuals demonstrate the greatest increases in
core temperature compared with paraplegic individuals, who in
turn demonstrate greater increases than able-bodied subjects
(12). During exercise in hot conditions, similar responses are
also observed with tetraplegic individuals being under a much
greater thermal strain than paraplegic individuals (22, 25)
because of the level of lesion being above the sympathetic
outflow, resulting in the absence or severe reduction of sweating capacity (12). Furthermore, during exercise in the heat,
paraplegic athletes demonstrate similar increase in core temperature compared with able-bodied bodied athletes during arm
crank ergometry (25) but at a much lower metabolic rate,
reflecting the decreased heat dissipation. The spinal cordinjured population, especially those individuals with tetraplegia, may therefore be considered to be at greater risk from
heat-related illness than able-bodied individuals.
Within the literature regarding human thermoregulation during exercise, a range of cooling strategies has been examined
(17). Such studies have been undertaken to determine methods
of reducing increases in body temperature during both lower
body (3, 7) and upper body exercise (27, 33) in hot conditions
as well as sports-specific environments (20). Techniques have
involved cooling before exercise (precooling), to delay increases in body temperature (20), or cooling during exercise, to
enhance the dissipation of heat gained from metabolic and/or
environmental sources (27). Although tetraplegic individuals
are known to be at greater risk of heat injury and that the main
contributor to heat strain in tetraplegic individuals is suggested
to be gains in heat from the environment (2, 26), little is known
regarding the reduction of heat strain in this population. When
spinal cord-injured subjects are cooled at rest, tetraplegic
individuals demonstrate greater decreases in core temperature
than paraplegic individuals and the able-bodied because of the
lack of sympathetically induced vasoconstriction and an inability to generate large amounts of metabolic heat from shivering
as a result of paralysis (5, 6, 12). It is possible that the absence
of heat retaining mechanisms in tetraplegic individuals may
enable a given cooling stimulus to be more effective than for
paraplegic and able-bodied subjects and would have a significant impact on the reduction of heat injury in this population
as well as improving the quality of life.
To the authors’ knowledge, only two studies have addressed
the topic of cooling strategies in the spinal cord injured (2, 13),
with both employing cooling strategies during exercise. Armstrong et al. (2) examined the effects of an ice-packet vest and
a refrigerated headpiece on 5-km performance time in a group
of wheelchair racers (including 4 paraplegic individuals and 1
tetraplegic individual). Although both cooling methods tended
Address for reprint requests and other correspondence: V. Goosey-Tolfrey,
Dept. of Exercise and Sport Science, The Manchester Metropolitan Univ.,
Crewe⫹Alsager Faculty, Alsager ST7 2HL, UK (E-mail: [email protected]).
The costs of publication of this article were defrayed in part by the payment
of page charges. The article must therefore be hereby marked “advertisement”
in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
spinal cord injury; core temperature; thermal strain; functional capacity
http://www. jap.org
8750-7587/05 $8.00 Copyright © 2005 the American Physiological Society
2101
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
Webborn, N., M. J. Price, P. C. Castle, and V. L. GooseyTolfrey. Effects of two cooling strategies on thermoregulatory responses of tetraplegic athletes during repeated intermittent exercise in
the heat. J Appl Physiol 98: 2101–2107, 2005. First published January
27, 2005; doi:10.1152/japplphysiol.00784.2004.—Athletes with spinal cord injury (SCI), and in particular tetraplegia, have an increased
risk of heat strain and consequently heat illness relative to able-bodied
individuals. Strategies that reduce the heat strain during exercise in a
hot environment may reduce the risk of heat illness. To test the
hypotheses that precooling or cooling during intermittent sprint exercise in a heated environment would attenuate the rise in core temperature in tetraplegic athletes, eight male subjects with SCI (lesions
C5–C7; 2 incomplete lesions) undertook four heat stress trials (32.0 ⫾
0.1°C, 50 ⫾ 0.1% relative humidity). After assessment of baseline
thermoregulatory responses at rest for 80 min, subjects performed
three intermittent sprint protocols for 28 min. All trials were undertaken on an arm crank ergometer and involved a no-cooling control
(Con), 20 min of precooling (Pre), or cooling during exercise (Dur).
Trials were administered in a randomized order. After the intermittent
sprint protocols, mean core temperature was higher during Con
(37.3 ⫾ 0.3°C) compared with Pre and Dur (36.5 ⫾ 0.6°C and 37.0 ⫾
0.5°C, respectively; P ⬍ 0.01). Moreover, perceived exertion was
lower during Pre (13 ⫾ 2; P ⬍ 0.01) and Dur (12 ⫾ 1; P ⬍ 0.01)
compared with Con (14 ⫾ 2). These results suggest that both precooling and cooling during intermittent sprint exercise in the heat
reduces thermal strain in tetraplegic athletes. The cooling strategies
also appear to show reduced perceived exertion at equivalent time
points, which may translate into improved functional capacity.
2102
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
METHODS
Subjects. Eight male wheelchair athletes (aged between 25 and 35
yr; 71.6 ⫾ 10.8 kg) volunteered to participate in the study after being
informed of the experimental procedures, which were approved by the
University Ethics Committee. Subjects were tetraplegic athletes (C5/
C6–C6/C7; 2 incomplete lesions), all being able to use their arms
during wheelchair propulsion but with impaired use of their hands. All
subjects trained and competed regularly in wheelchair tennis (n ⫽ 4)
and rugby (n ⫽ 4) at either the national or international level and were
familiar with arm-crank exercise. Subjects visited the laboratory on
four separate occasions. During the first visit to the laboratory,
anthropometric measurements were taken [sum of 4 skinfolds; Harpenden Instruments, West Sussex, UK, as described by Durnin and
Womersley (9)] followed by a force velocity test and an incremental
arm-crank test to volitional exhaustion. After 2-h chaperoned rest,
subjects also undertook an 80-min resting heat exposure. The remaining visits involved intermittent exercise protocols with three different
cooling procedures.
Instrumentation. Exercise testing was performed on a modified
cycle ergometer (Ergomedic 620, Monark, Varberg, Sweden) adapted
for upper body exercise that allowed athletes to remain in their
everyday wheelchairs for testing. Because subjects demonstrated
impaired hand function, assistance in gripping the hand cranks was
provided via taping where necessary. Power measuring cranks (SRM,
Welldorf, Germany) were fitted to the ergometer to record power
output continuously at a sampling rate of 0.5 Hz.
Physiological measures. Subjects ingested the telemetry pill (HQ
Palmetto, Fl) for the measurement of core body temperature, 8.0 ⫾
2.3 h before each testing condition, in accordance with Sparling et al.
(30) to ensure reliable values. The telemetry pill detects surrounding
temperature and transmits a temperature variable signal via short
electromagnetic waves to a hand held recorder. This technology has
been deemed reliable during hyperthermia (21) and has demonstrated
good response times to detect temperature change by Mittal et al. (19).
Body mass in minimal clothing was determined before and after
testing for an indication of nonurine fluid loss. Thermistors (Grant
Instruments, Cambridge, UK) were positioned for measures of skin
temperature at standard positions (28) on the chest, upper arm, thigh,
and calf. Values were recorded by a Grant Squirrel meter logger (1000
J Appl Physiol • VOL
Series, Grant Instruments, Cambridge, UK). Heart rate was continually monitored (Polar Sports Tester, Kempele, Finland). Subjective
measures for rating of perceived exertion (4) and thermal sensation
(31) were also recorded.
Baseline measures were recorded after a 15-min period to allow
stabilization of thermistors. During the 20-min precooling maneuver
and time-matched period for the control and during conditions, all
variables were recorded at 2-min intervals. For logistical reasons,
during the intermittent sprint protocol, all variables were recorded at
1 min of each 2-min exercise block to gauge the responses during the
active recovery section of the protocol. Power output was measured
continuously. Peak power output during each 5-s sprint was recorded
as the highest single value during each 5-s sprint. Mean work done for
each 5-s sprint was calculated from the highest 3-s average for mean
power output during each sprint. On completion of each intermittent
sprint protocol, when subjects felt they could no longer continue, or
the safety limit of a high core temperature was reached (39.3°C or a
2°C increase from rest), the trial was terminated.
Mean skin temperature was calculated using the formula of Ramanathan (28), and heat storage was calculated using the formula of
Havenith et al. (15):
Heat storage ⫽ 共0.8⌬Tcore ⫹ 0.2⌬MST兲 䡠 Cb,
where Cb is the specific heat capacity of the body tissue (3.49
J 䡠 g⫺1 䡠 °C⫺1). Values were calculated from changes in telemetry pill
core temperature (⌬Tcore) and mean skin temperature (⌬MST) from
resting values at the end of the precooling maneuver and the end of the
intermittent sprint protocol.
Experimental procedure. Subsequent to medical screening by a
physician, all subjects refrained from vigorous exercise, caffeine, and
alcohol for 24 h before reporting to the laboratory for the first time.
Before all testing protocols, subjects provided a urine sample for the
assessment of hydration status via urine specific gravity [Cambur10
Test, Roche Diagnostics, Mannheim, Germany (1)].
The force-velocity test consisted of three maximum-effort sprints
of 5-s duration against a resistance of 2, 3, and 4% of body mass.
Sprints were interspersed by 5-min active recovery on the unloaded
ergometer. The resistance that yielded the highest peak power output
was then used during subsequent tests. After 15-min rest, subjects
completed a continuous incremental exercise test to determine peak
oxygen uptake (V̇O2 peak). This test involved increases in workload of
5 W every 2 min from an initial workload of 35 W at a cadence of 60
rpm. Expired air was collected during the last minute of each stage by
using the Douglas bag technique and analyzed for oxygen and carbon
dioxide content (Servomex, Crowborough, UK) and expired volume
(Harvard Dry Gas Meter, Scientific and Research Instruments, Kent,
UK). Heart rate was continually monitored After the V̇O2 peak test and
2-h chaperoned rest, subjects rested in an environmental chamber with
the ambient temperature and relative humidity set at 32.0 ⫾ 0.1°C,
and 50.0 ⫾ 0.1%, respectively, for 80 min to assess baseline thermoregulatory responses and the level of heat strain.
All exercise tests undertaken during the three remaining laboratory
visits occurred inside the environmental chamber on separate days and
in a randomized order. The environmental conditions were the same
as for the resting heat exposure. Trials were conducted at the same
time of day to negate circadian variation (16) and consisted of a
repeated-measures design where subjects served as their own controls.
The three trials were consisted of an intermittent sprint protocol with
no cooling (Con); an intermittent sprint protocol preceded by a 20-min
precooling maneuver (Pre) in which subjects wore a commercially
available ice vest (Arctic Heat Products) covering the torso before
exercise only; and an intermittent sprint protocol with subjects wearing the ice vest during the warm-up and intermittent sprint protocol
only (Dur). The warm-up before each trial consisted of arm crank
exercise at ⬃50% peak power output from the V̇O2 peak test (60 rpm,
29 –37 W).
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
to show cooler rectal, skin, and mean body temperatures, no
significant differences were observed between trials. The authors concluded that local cooling was ineffective because heat
storage, although reduced, was not prevented. Hagobian et al.
(13) examined the use of a foot-cooling device in a group of
spinal cord-injured men (C5 to T5) during exercise in hot
conditions. Foot cooling was successful in attenuating the rise
in core temperature during exercise (1.0 ⫾ 0.2°C) compared
with a no-cooling control (1.6 ⫾ 0.2°C). Although these
studies have provided useful insights into the use of potential
cooling strategies during exercise in the spinal cord injured,
subjects were not athletes and the exercise employed was of an
aerobic nature. These conditions do not necessarily reflect the
intermittent- and high-intensity nature of many wheelchair
sports and represent exercise conditions that need to be addressed. Furthermore, no study has yet reported the use of
cooling strategies in a large and homogenous group of tetraplegic individuals. Therefore, the aim of this study was to describe
the effects of precooling and cooling on the responses during
several intermittent high-intensity exercise bouts over 28 min
in tetraplegic individuals. It was hypothesized that precooling
would delay the onset of increases in body temperature,
whereas cooling during exercise would offset gains in heat
during exercise.
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
RESULTS
The physiological parameters obtained from both the forcevelocity and peak aerobic arm ergometry are presented in
Table 1. These values were found to be consistent with those
previously reported (26) and unpublished data from other
researchers using the SRM power crank device.
During 80 min of passive rest in hot conditions, core body
temperature increased from resting values (36.8 ⫾ 0.1°C) to
37.3 ⫾ 0.1°C (P ⬍ 0.01). Mean skin temperature also increased from 32.0 ⫾ 0.2°C at the start of the rest period to
34.8 ⫾ 0.2°C by the end of the 80-min period (P ⬍ 0.01). By
28 min of exposure (a time period comparable to the intermittent sprint duration), heat storage was 1.06 ⫾ 0.5 J/g. Mean
heart rate was 65 ⫾ 2 beats/min and did not change throughout
the 80-min rest. Body mass was not reduced from baseline
values during rest in the heat.
Precooling maneuver. The precooling maneuver reduced
core temperature from rest (36.6 ⫾ 0.1°C) by 0.3 ⫾ 0.1°C
(P ⬍ 0.05; Fig. 1) and mean skin temperature by 1.7 ⫾ 0.4°C
(P ⬍ 0.01; Fig. 2). Heat storage after the precooling period was
⫺2.53 ⫾ 0.35 J/g. Heart rate was not changed during precooling, although ratings of thermal sensation were lowered from
rest (3.5 ⫾ 0.4) by 20 min of precooling (1.5 ⫾ 0.2, P ⬍ 0.01;
Fig. 3). No differences were observed for any variables during
the time-matched period of precooling for Con or Dur.
Warm-up. During the warm-up, core temperature did not
increase from initial values in any condition, although mean
core temperature tended to be lower for Pre (36.1 ⫾ 0.2°C)
than both Con and Dur (36.6 ⫾ 0.1°C and 36.7 ⫾ 0.1°C,
respectively; P ⬍ 0.05). Mean skin temperature increased from
baseline values by minute 5 of the warm-up in all conditions
(2.5 ⫾ 0.2°C Con, 1.7 ⫾ 0.3°C Pre, and 1.5 ⫾ 0.2°C Dur; P ⬍
0.01). Furthermore, mean skin temperature for Pre and Dur
was lower than Con at this time point and for the remainder of
the warm-up (P ⬍ 0.01). Heat storage during the warm-up for
Con was 2.06 ⫾ 0.07 J/g, and although lower for Pre (1.35 ⫾
0.1 J/g) and Dur (1.31 ⫾ 0.23 J/g), the reduction was not
significant (P ⫽ 0.67). Mean heart rate was higher during
warm-up for Con (86 ⫾ 4 beats/min) compared with Pre (82 ⫾
3 beats/min) and Dur (75 ⫾ 3 beats/min; P ⬍ 0.01). The
difference between Pre and Dur was also significant (P ⬍ 0.01;
Fig. 3). Ratings of thermal sensation were similar across
conditions during the warm-up and increased from the first
minute of the warm-up (3.5 ⫾ 0.2 Con, 3.5 ⫾ 0.4 Pre, and
3.0 ⫾ 0.4 Dur) to the third minute (4.5 ⫾ 0.2 Con, 4.0 ⫾ 0.2
Pre, and 4.0 ⫾ 0.2 Dur; P ⬍ 0.05). These increases were
sustained until the end of the warm-up period (P ⬍ 0.05; Fig. 3).
Thermoregulatory, cardiovascular, and subjective responses during the intermittent sprint protocol. Core temperature on completion of the warm-up before the intermittent
sprint protocol was not different between Con, Pre, and Dur at
36.7 ⫾ 0.3, 36.1 ⫾ 0.2, and 36.7 ⫾ 0.1°C, respectively. During
the intermittent sprint protocol, core temperature was higher
during Con (37.3 ⫾ 0.1°C) compared with Pre (36.5 ⫾ 0.2°C;
main effect, P ⬍ 0.01) and Dur (37.0 ⫾ 0.2°C; P ⬍ 0.01). The
difference between Pre and Dur was also significant (main
effect; P ⬍ 0.01; Fig. 1). There was a significant increase in
core temperature after 7 min for the Dur condition (P ⱕ 0.01),
which was delayed until 9 min for the Con and Pre conditions
(P ⱕ 0.01). Throughout Pre and Dur, core temperature was
lower than for Con (P ⬍ 0.01). Furthermore, Pre also resulted
in lower core temperature at every time point than Dur (P ⬍
0.01). Core temperature on completion of the intermittent
sprint protocol was different between all conditions at 37.9 ⫾
0.1°C for Con compared with 37.2 ⫾ 0.2 and 37.4 ⫾ 0.2°C for
Pre and Dur, respectively (P ⬍ 0.01). However, the rate of
temperature increase throughout Dur (0.028 ⫾ 0.04°C/min)
was lower than Con (0.041 ⫾ 0.004°C/min) and Pre (0.039 ⫾
0.07°C/min; P ⬍ 0.05).
Mean skin temperature was not different between trials for
Con or Pre; however, values were lower for Dur compared
with Con (32.2 ⫾ 0.2°C and 34.0 ⫾ 0.1°C, respectively; main
effect, P ⬍ 0.05). In all conditions, skin temperature increased
from the first minute of the intermittent sprint protocol by 7
min (P ⬍ 0.01; Fig. 2) and remained elevated throughout. For
Table 1. Physiological characteristics of the wheelchair athletes
Subject
BM, kg
SS, mm
PPO, W
Aerobic PPO, W
V̇O2 peak, l/min
HRpeak, beats/min
Mean ⫾ SE
Maximum
Minimum
71.6 ⫾ 3.8
93.5
57.0
57.7 ⫾ 4.1
71.6
37.1
220 ⫾ 22
307
134
70 ⫾ 5
85
49
0.96 ⫾ 0.06
1.18
0.66
142 ⫾ 4
168
115
Values are for 8 subjects. BM, body mass; SS, sum of 4 skinfolds; PPO, peak power output from force-velocity test; Aerobic PPO, PPO from the incremental
test; V̇O2 peak, peak oxygen uptake; HRpeak, peak heart rate.
J Appl Physiol • VOL
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
The ice vest was frozen overnight before testing in a ⫺20°C freezer
and weighed 1.4 kg. Before baseline measures being recorded in all
conditions, subjects rested for 15 min in temperate conditions (20.0 ⫾
0.1°C and 45.0 ⫾ 0.1% relative humidity). For the Con condition,
subjects remained resting in the same conditions for a further 20 min
before entering the environmental chamber. For the Pre condition
after the baseline period, subjects wore the ice vest for 20 min, after
which the subjects removed the vest and entered the environmental
chamber. For the Dur condition, once baseline measures had been
recorded, subjects rested for 20 min as in Con before putting on the ice
vest and immediately entering the environmental chamber. The intermittent sprint protocol involved fourteen 2-min exercise periods, each
consisting of a 10-s passive rest, a 5-s maximal sprint from a
stationary start against the optimal resistance from the force-velocity
test, and 105 s of active recovery at 35% V̇O2 peak. No fluid intake was
permitted during any of the testing. Subjects wore lightweight tracksuit trousers and training shoes for all tests. The use of a 28-minduration intermittent sprint protocol was based on pilot work and
represented an exercise duration that all subjects were able to achieve.
All data were checked for normality, and sphericity was assumed
using the Hunh-Feldt method. Paired data from each intermittent
sprint protocol was analyzed by using a two-way ANOVA with
repeated measures (condition ⫻ time). Significance was accepted at
the P ⬍ 0.05 level. Where significance was obtained, Tukey’s honestly significant difference post hoc test was undertaken. All data were
analyzed by using a standard statistical package (SPSS Version 11.0)
and are reported as means ⫾ SE.
2103
2104
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
time-matched data points during the intermittent sprint protocol, mean skin temperature for Pre and Dur conditions were
lower for Con (P ⬍ 0.01). Furthermore, each data point for the
Dur condition was lower than Pre throughout the intermittent
sprint protocol (Fig. 2; P ⬍ 0.01). Individual skin temperatures
increased from resting values during each intermittent sprint
protocol trial (P ⬍ 0.05). Both thigh and calf skin temperatures
were cooler than chest and arm skin temperatures at rest, after
warm-up, and throughout the three intermittent sprint protocol
trials.
Heat storage during the intermittent sprint protocol was not
different between Con (3.62 ⫾ 0.4 J/g), Pre (4.17 ⫾ 0.4 J/g),
and Dur (3.15 ⫾ 0.35 J/g; P ⫽ 0.39). Heart rate increased from
minute 1 to minute 13 (P ⬍ 0.05) during each intermittent
sprint protocol and was not different across conditions. Change
in body mass was not different between Con (0.15 ⫾ 0.1 kg),
Pre (0.01 ⫾ 0.3 kg), and Dur (0.05 ⫾ 0.0 kg; P ⫽ 0.71).
For the Dur condition, thermal sensation was lower (5.0 ⫾
0.2) than Con (6.0 ⫾ 0.2, main effect; P ⬍ 0.05) but not
different from Pre (5.5 ⫾ 0.2; Fig. 3). Compared with values at
1 min, thermal sensation was elevated for the Con and Pre
conditions (5.0 ⫾ 0.2 and 4.5 ⫾ 0.2, respectively) at 13 min
(6.0 ⫾ 0.2 and 5.5 ⫾ 0.4, respectively; P ⬍ 0.01). However,
for the Dur condition, a significant increase did not occur until
15 min (5.5 ⫾ 0.4) from 1 min (4.5 ⫾ 0.4, P ⬍ 0.01; Fig. 3).
Ratings of perceived exertion were lower during Pre (13.0 ⫾
0.7, P ⬍ 0.01; Fig. 4) and Dur (12.0 ⫾ 0.4, P ⬍ 0.01; Fig. 4)
compared with Con (14.0 ⫾ 0.7). During the intermittent sprint
protocol, significant increases in perceived exertion were observed at 11 min for Con, 13 min for Pre, and 15 min for Dur.
From 18 min onward, values were lower for Dur than Con
(P ⬍ 0.01; Fig. 4). No significant differences were seen across
conditions for overall mean work done.
DISCUSSION
The aim of this study was to examine the effects of precooling and cooling during intermittent high-intensity exercise in
tetraplegic individuals. Physiological and thermoregulatory reJ Appl Physiol • VOL
sponses supported the use of both cooling strategies in offsetting thermal strain during 28 min of exercise.
Before any exercise trials, each subject’s thermal strain was
assessed during a resting heat exposure over a comparable
duration to the exercise trials in the present study and a
previous study of spinal cord-injured individuals (26). Over the
entire 80-min duration, core temperature, as measured via the
telemetry pill, increased by ⬃0.5°C with a corresponding
increase in mean skin temperature of 2.4°C. The increase in
core temperature was less than observed by previous studies of
the spinal cord injured employing oral, aural, and rectal temperature (12, 29, 32) and probably reflects not only the greater
environmental temperature of previous exposures (35–38°C)
but also the trained nature of the subject group, which may
elicit improvements in heat tolerance (26). Furthermore, no
change in body mass was observed during the exposure demonstrating the lack of sweating capacity within the group.
The precooling maneuver at rest in the cool environment
effectively reduced core temperature before the warm-up period. However, this was not as extreme as whole body cooling
techniques such as immersion (18) or a 60-min cold shower
(7), which have been employed with able-bodied subjects but
are less practical for most sporting situations. The present
study reduced mean skin temperature by ⬃1.5°C, whereas a
similar technique employing able-bodied athletes over a
shorter duration in a warm environment (30°C) reported a
reduction in mean skin temperature by over 4°C and tympanic
temperature (infrared method) by 0.9°C (20). It is possible that
able-bodied subjects in warm conditions would have had a
large afferent stimulus for vasodilation from the neurologically
intact whole body skin surface area. This would result in a
much greater stimulus for increased cutaneous blood flow
overriding any local vasoconstrictor stimulus from the relatively small surface area cooled by the ice vest. Consequently,
blood would still flow through the cooled skin areas, returning
to the central circulation. It is likely that this would not occur
for tetraplegic subjects in the present study because of the lack
of a large vasodilatory stimulus from the majority of the skin
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
Fig. 1. Core temperature during the precooling maneuver, warm-up, and intermittent sprint protocol for the no-cooling control (Con), 20 min of precooling (Pre),
or cooling during exercise (Dur) conditions in a hot, humid environment. a Significant difference between Con and Pre, P ⬍ 0.05. b Significant difference between
Con and Dur, P ⬍ 0.05. c Significant difference between Pre and Dur, P ⬍ 0.05. *Significant difference from rest, P ⬍ 0.05.
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
2105
surface to drive blood through the cooled cutaneous circulation. When a similar ice vest to the one in the present study was
employed for just 5 min after warm-up, little change in rectal
or mean skin temperature was observed (8), demonstrating that
the duration of cooling may have been too short even for
able-bodied subjects to benefit. These differences in cooling
potential are also possibly due to the greater surface area
cooled (20) and the use of the Ramanathan mean skin temperature formula (28), possibly masking any local cooling effect
(27). Interestingly, in the present study,⫹ chest temperature
was decreased, on average, ⬃4°C, which is consistent with that
observed by Myler et al. (20). However, although precooling
was effective in the tetraplegic athletes studied, the reduction
in body temperature during Pre would not be large enough to
offset the gain in heat during the 80-min resting heat exposure.
During the warm-up period, heat storage during the two
cooling trials was similar and ⬃65% of that observed for Con.
This suggests that the effectiveness of the precooling strategy
was maintained at a similar level as wearing the ice vest during
warm-up. Although this represents only a short duration of
time, such a time factor may be important for competitive
situations or where limited time for cooling athletes is available. Consequently, subjects began the exercise protocol with
the same body heat content for the Pre and Dur trials.
During exercise, core temperature was lower during both
cooling trials compared with the no-cooling control. Furthermore, for a given time point, core temperature was lower
during Pre compared with Dur, suggesting that precooling
reduced the absolute increase in core temperature. However,
the rate of increase in core temperature was slower for Dur
compared with Pre and Con, which were similar. As a result,
similar core temperatures were observed at the end of exercise
for both cooling protocols. Consequently, precooling offset the
absolute increase in core temperature, whereas wearing the ice
vest during exercise reduced the gain in core temperature and
may be due to the following. In the absence of sympathetically
induced vasoconstriction, cutaneous blood would not be directed to the body core during Pre until the warm-up and
Fig. 3. Thermal sensation scores during the precooling maneuver, warm-up, and intermittent sprint protocol for the Con, Pre, and Dur conditions in a hot, humid
environment. a Significant difference between Con and Pre, P ⬍ 0.05. c Significant difference between Pre and Dur, P ⬍ 0.05. *Significant difference from rest,
P ⬍ 0.05.
J Appl Physiol • VOL
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
Fig. 2. Mean skin temperature during the precooling maneuver, warm-up, and intermittent sprint protocol for the Con, Pre, and Dur conditions in a hot, humid
environment. a Significant difference between Con and Pre, P ⬍ 0.05. b Significant difference between Con and Dur, P ⬍ 0.05. c Significant difference between
Pre and Dur, P ⬍ 0.05.
2106
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
Fig. 4. Ratings of perceived exertion during the intermittent
sprint protocol for the Con, Pre, and Dur conditions in a hot,
humid environment. b Significant difference between Con
and Dur, P ⬍ 0.05.
J Appl Physiol • VOL
aim of cooling in this population during high-intensity intermittent exercise may shift toward offsetting gains in core
temperature of metabolic origin. Further studies examining
intermittent sprint type activities would therefore be of interest.
It must be emphasized though that the group studied were
trained athletes and may demonstrate an increased heat tolerance from regular increases in body temperature during training (26). Sedentary or less-trained tetraplegic subjects may
well be at a greater risk of heat injury than those studied. This
is further illustrated when considering that the amount of heat
stored during Con was similar to that gained during 60 min of
continuous exercise in similar conditions for able-bodied athletes (25).
Perceptions of thermal sensation at the end of exercise were
similar for both Pre and Dur with ratings of “warm” compared
with the Con trial where ratings of “hot” were reported. The
latter values are similar to those reported for able-bodied
subjects during arm crank ergometry in hotter conditions
(39°C) (27), further illustrating the reduced thermoregulatory
capacity in tetraplegic individuals. Wearing the ice vest during
exercise in the heat also delayed the increase in perceptions of
thermal strain by 2 min compared with Pre cooling. The similar
values between trials after this point are most likely due to the
ice vest losing its effectiveness as the ice strips thawed, a factor
commented on by the majority of subjects. It is likely that both
the reduced thermal and cardiovascular strain contributed to
the reduced perception of effort during the cooling trials.
Limitations. Although the two subjects with incomplete
lesions did demonstrate the greatest V̇O2 peak (1.18 and 1.20
l/min), this was not the same for peak power output where,
unlike submaximal responses, little relationship between completeness of lesion and peak power output was evident. For
these two subjects, however, differences in V̇O2 peak were
essentially negligible compared with the rest of the group and
would not have resulted in different metabolic rates (i.e., heat
production) during the 35% V̇O2 peak exercise component between sprints. Consequently, because the exercise was a sprintbased protocol, it is unlikely that completeness of lesion would
affect heat production per se. However, the incomplete subjects
were two of only three subjects to demonstrate any sweating
responses during the resting exposure. Although this cannot be
discounted in assessing the thermoregulatory data, no obvious
link appears to exist within our data between completeness of
lesion and thermal parameters. Although previous authors have
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
exercise protocol began elevating heart rate to drive the cooled
cutaneous blood to the central circulation, thus maintaining a
cool core. This process would likely continue during exercise
and heat exposure until skin temperature increased to a level
where cutaneous blood no longer remained cool. Conversely,
wearing the ice vest during exercise would enable blood
returning to the central circulation from the skin to be continually cooled, thus preventing the rapid rate of increase in core
temperature observed for Con. What must be considered,
however, is how long the ice vest remains cold and how long
the precooled skin takes to rewarm. These factors may be of
importance in determining the duration of exercise capacity in
this population. It is anticipated though, that in conditions of
greater environmental stress the effectiveness of both strategies
would be reduced.
Skin temperature demonstrated similar responses during
each trial to those observed for core temperature. However, in
the Dur trial, a slower increase in temperature was demonstrated during exercise, and in the Pre trial, a systematic
decrease was demonstrated due to the direct application of the
cooling stimuli. Considering the core and skin temperature
responses combined, the Pre strategy demonstrated central
cooling and offset the subsequent gain in core temperature
during exercise, whereas the Dur protocol initially demonstrated peripheral cooling, facilitating direct heat transfer from
the body core to the periphery. As regards heat flow, regional
differences are likely to have occurred. For example, in all
trials, the arms, not covered by the ice vest, reached skin
temperatures similar to those of core temperature, subsequently
retarding heat loss from the core to the periphery. Lower body
skin temperatures of the thigh and calf, which were the coolest
of any site at rest (28.5 and 26°C, respectively), increased to
environmental temperature (31–32°C) during exercise, which
would allow heat flow from the core to periphery and possible
dry heat exchange to the environment.
The heat stored during Con represents both the metabolic
heat production and that gained from the environment. Compared with the 28-min point during the resting exposure, it
appears that two-thirds of the heat gained during Con was from
metabolic heat production rather than the environment. If the
exercise had been of a more aerobic nature, the majority of heat
gained by the individuals may well have been from environmental sources, which would be consistent with previous
studies involving tetraplegic athletes (2, 11). Consequently, the
COOLING AND RESPONSES OF TETRAPLEGIC ATHLETES IN THE HEAT
ACKNOWLEDGMENTS
We are grateful to all members of the British Paralympic Sport Science and
Medicine Steering Group, David Lasini, Dawn Newbery, and Jeremy Moody
for input toward the development of the project.
GRANTS
This study was supported by United Kingdom Sports Institute Grant
E161-03.
REFERENCES
1. Armstrong LE, Maresh CM, Castellani JW, Bergeron MF, Kenefick
RW, LaGasse KE, and Riebe D. Urinary indices of hydration status. Int
J Sport Nutr 4: 265–279, 1994.
2. Armstrong LE, Maresh CM, Riebe D, Kenefick RW, Castellani JW,
Senk JM, Echegaray M, and Foley MF. Local cooling in wheelchair
athletes during exercise-heat stress. Med Sci Sports Exerc 27: 211–216,
1995.
3. Booth J, Wilsmore BR, Macdonald AD, Zeyl A, McGhee S, Calvert D,
Marino F, Storlien LH, and Taylor NAS. Whole body pre-cooling does
not alter human muscle metabolism during sub-maximal exercise in the
heat. Eur J Appl Physiol 84: 587–590, 2001.
4. Borg GAV. Perceived exertion as an indicator of somatic stress. Scand J
Rehabil Med 2: 92–98, 1970.
5. Downey JA, Chiodi HP, and Darling RC. Central temperature regulation in the spinal man. J Appl Physiol 22: 91–94, 1967.
6. Downey JA, Huckaba CE, Kelley PS, Tam HS, Darling RC, and Cheh
HY. Thermoregulatory responses to deep and superficial cooling in man.
J Appl Physiol 27: 209 –212, 1969.
7. Drust B, Cable NT, and Reilly T. Investigation of the effects of the
pre-cooling on the physiological responses to soccer specific intermittent
exercise. Eur J Appl Physiol 81: 11–17, 2000.
J Appl Physiol • VOL
8. Duffield R, Dawson B, Bishop D, Fitzsimmons M, and Lawrence S.
Effect of wearing an ice cooling jacket on repeated sprint performance in
warm/humid conditions. Br J Sports Med 37: 164 –169, 2003.
9. Durnin JVGA and Womersley J. Body fat assessed from total body
density and its estimation from skinfold thickness: measurements on 481
men and women aged from 16 to 72 years. Br J Nutr 32: 77–97, 1974.
10. Freund PR, Brengelmann GL, Rowell LB, and Halar E. Attenuated
skin blood flow response to hyperthermia in paraplegic men. J Appl
Physiol 56: 1104 –1109, 1984.
11. Gass EM, Gass GC, and Gwinn TH. Sweat rate and rectal temperatures
in tetraplegic men during exercise. Sports Med Training Rehabil 3:
243–249, 1992.
12. Guttman L, Silver J, and Wyndham CH. Thermoregulation in spinal
man. J Physiol 142: 406 – 419, 1958.
13. Hagobian TA, Jacobs KA, Kiratli J, and Friedlander AL. Foot cooling
reduces exercise-induced hyperthermia in men with spinal cord injury.
Med Sci Sports Exerc 36: 411– 417, 2004.
14. Hamilos DL, Nutter D, Gershtenson J, Redmond DP, Di Clementi JD,
Schmaling KB, Make BJ, and Jones JF. Core body temperature is
normal in chronic fatigue syndrome. Biol Psychiatry 43: 293–302, 1998.
15. Havenith G, Inoue Y, Luttikholt V, and Kenney WL. Age predicts
cardiovascular, but not thermoregulatory responses to humid heat stress.
Eur J Appl Physiol 70: 88 –96, 1995.
16. Hill DW, Hill CM, Fields KL, and Smith JC. Effects of jet lag on factors
related to sports performance. Can J Appl Physiol 18: 91–103, 1993.
17. Marino F. Methods, advantages, and limitations of body cooling for
exercise performance. Br J Sports Med 36: 89 –94, 2002.
18. Marsh D and Sleivert G. Effect of precooling on high intensity cycling
performance. Br J Sports Med 33: 393–397, 1999.
19. Mittal BB, Sathiaseelan V, Rademaker AW, Pierce MC, Johnson PM,
and Brand WN. Evaluation of an ingestible telemetric temperature sensor
for deep hyperthermia applications. Int J Radiat Oncol Biol Phys 21:
1353–1361, 1991.
20. Myler G and Hahn AG, and Tumilty DMcA. The effects of preliminary
skin cooling on performance of rowers in hot condition. Excel 6: 17–21,
1989.
21. O’Brien C, Hoyt RW, Buller MJ, Castellani JW, and Young AJ.
Telemetry pill measurement of core temperature in humans during active
heating and cooling. Med Sci Sports Exerc 30: 468 – 472, 1998.
22. Petrofsky JS. Thermoregulatory stress during rest and exercise in heat in
patients with a spinal cord injury. Eur J Appl Physiol 64: 503–507, 1992.
23. Price MJ and Campbell IG. Thermoregulatory responses of able-bodied
and paraplegic athletes to prolonged upper body exercise. Eur J Appl
Physiol 76: 552–560, 1997.
24. Price MJ and Campbell IG. Thermoregulatory and physiological responses of wheelchair athletes to prolonged arm crank and wheelchair
exercise. Int J Sports Med 20: 457– 463, 1999.
25. Price MJ and Campbell IG. Thermoregulatory responses of able-bodied,
upper body trained athletes to prolonged arm crank exercise in cool and
hot conditions. J Sports Sci 20: 519 –527, 2002.
26. Price MJ and Campbell IG. Effects of spinal cord lesion level upon
thermoregulation during exercise in the heat. Med Sci Sports Exerc 35:
1100 –1107, 2003.
27. Price MJ and Mather MI. The effects of two cooling strategies during
prolonged arm crank exercise in hot conditions. Aviat Space Environ Med
75: 220 –226, 2004.
28. Ramanathan NL. A new weighting system for mean surface temperature
of the human body. J Appl Physiol 19: 531–533, 1964.
29. Ready AE. Responses of quadriplegic athletes to maximal and submaximal exercise. Physiother Can 36: 124 –128, 1984.
30. Sparling PB, Snow TK, and Millard-Stafford ML. Monitoring core
temperature during exercise: ingestible sensor vs rectal thermistor. Aviat
Space Environ Med 64: 760 –763, 1993.
31. Toner MM, Drolet LL, and Pandolf KB. Perceptual and physiological
responses during exercise. Percept Mot Skills 62: 211–220, 1986.
32. Totel GL, Johnson RE, Fay FA, Goldstein JA, and Schick J. Experimental hyperthermia in traumatic quadriplegia. Int J Biometeorol 15:
346 –355, 1971.
33. Young AJ, Sawka MN, Epstein Y, Decristofano B, and Pandolf KB.
Cooling different body surfaces during upper and lower body exercise.
J Appl Physiol 63: 1218 –1223, 1987.
98 • JUNE 2005 •
www.jap.org
Downloaded from http://jap.physiology.org/ by 10.220.33.1 on July 12, 2017
observed sweating in this population, it has been either limited
(11) or ineffective (22) and is unlikely to have affected the
thermal parameters in our population. Furthermore, all core
temperature responses for these subjects were within 1 SD of
the mean response; inclusion of their data, therefore, did not
alter the results of the statistical analysis.
A further point to comment on is the use of the telemetry pill
technique. This mode is useful for monitoring transient changes
in core temperature of tetraplegic athletes, without causing any
discomfort that may be associated with esophageal thermometry. Although Himilos et al. (14) concluded that the telemetry
pill was faster to respond to changes in body temperature than
rectal temperature, this technique is not without limitations,
such as difficulty in determining the exact location of the
telemetry pill within the gastrointestinal tract. However, the
methods employed within the present investigation should
have delimited this potential error by following previous methodological recommendations ensuring reliable data up to 12 h
postingestion (20, 29) and being concerned primarily with the
cummulative heat gain during each trial.
In conclusion, both cooling strategies facilitated reduced
thermal and cardiovascular strain that may translate into improved functional capacity and reduced perceptual responses of
trained tetraplegic individuals. Interestingly, the high-intensity
nature of the intermittent sprint protocol may have elicited a
greater contribution to heat gain from metabolism than previous continuous exercise investigations. Consequently, the particular cooling strategy employed may depend on the specific
exercise scenario to be undertaken and whether peripheral or
central cooling is the greater requirement.
2107